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A Review of Forty-Five Years Study of Hiroshima and Nagasaki Atomic Bomb Survivors

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A Review of Forty-Five Years Study of Hiroshima and Nagasaki Atomic Bomb Survivors A Review of Forty-Five Years Study of Hiroshima and Nagasaki Atomic Bomb Survivors II. BIOLOGICAL EFFECTS Follow-up Studies of Breast Cancer Incidence among Atomic Bomb Survivors MASAYOSHI TOKUNAGA1,2, CHARLES E. LAND3 AND SHOJI TOKUOKA1 Department of EpidemiologicPathology, Radiation Effects Research Foundation, Hiroshima1 732, Japan 2Department of Pathology, Kagoshima Municipal Hospital, Kagoshima 892, Japan 3Radiation Epidemiology Branch, National Cancer Institute, U.S.A. Breast cancer/Atomic bombing/Radiation/Carcinogenesis/Epidemiology INTRODUCTION Although breast cancer rates among Japanese women are normally very low compared to other countries, the excess risk associated with exposure to ionizing radiation, as observed in the Life Span Study Sample (LSS) sample of the Radiation Effects Research Foundation (RERF), Hiroshima and Nagasaki, is fully as high as that seen in medically-irradiated Western populations. This combination of a high radiation-related excess and a relatively low baseline level of risk means that the LSS cohort is especially informative about radiation-induced breast cancer. In this paper we review the results of published studies of breast cancer incidence and mortality among A-bomb survivors, their relationship to findings from studies of other irradiated populations, and their possible implications for radiation-induced cancer in general. We conclude with an overview of current studies, which extend beyond the investigation of risk as a function of radiation dose. BACKGROUND Breast cancer incidence among A-bomb survivors The first study to find an excess breast cancer risk among A-bomb survivors was reported by Wanebo et al.t) in 1967. This was only two years after Mackenzie2) had demonstrated an association with x-ray exposure from multiple chest fluoroscopies used to monitor pneumothorax treatment for tuberculosis in a Nova Scotia sanitorium. Wanebo's study was limited to the clinical sub-sample of the LSS sample, that is, the subgroup that has been routinely solicited for biennial clinical examinations at the Atomic Bomb Casualty Commission and its successor, the RERF, since 1958. It is of some interest, in view of the numbers in more recent studies, to note that Wanebo's finding was based on only 27 breast cancer cases diagnosed during the period 1950-66 and, in particular, on only 9 histologically verified cases with estimated exposures over 0.9 Gy T65D3> tissue Kerma compared with 4.3 cases expected in the absence of a dose response. The report by Mackenzie was based on 13 cases in 271 patients vs. one case in 570 patients who had not been given fluoroscopy; most of the irradiated patients had received cumulative breast tissue doses far higher than all but a very few A-bomb survivors. McGregor et al.4) extended the A-bomb survivor investigation to the entire LSS sample, and reported 231 breast cancers diagnosed during the period 1950-69. Ascertainment was based upon death certificates, autopsy records, the tumor registries of Hiroshima and Nagasaki, and ABCC records. A strong, approximately linear dose response was observed: for all exposure ages combined the estimated excess relative risk at 1 Gy breast tissue dose (see Kerry was about 1.1 ± 0.26. Of special interest from today's vantage point was the evidence of a downward gradient in risk with increasing age at exposure: the estimated excess relative risks at 1 Gy were approximately 2.5 ± 0.8, 0.7±0.3, 0.18±0.24, and 0.35±0.42 for exposure ages 10-19, 20-34, 35-49, and 50+, respectively. Only one (non-exposed) case was observed among women who were under 10 years of age ATB (i.e., at the time of the bombings), whose maximum age in 1969 was only 34. Also of interest was an apparent lack of dependence among breast cancer cases between radiation dose and time from exposure until cancer diagnosis. Tokunaga et al.6), in extending the LSS sample incidence series through September, 1974, introduced more exhaustive methods of case ascertainment using local sources of diagnostic information such as hospitals and clinics. A total of 360 cases was reported, including only 5 among women under 10 years of age ATB. Highly significant dose responses were found for each of the cohorts 10-19, 20-29, and 30-39 years of age ATB, but there was actually a statistically significant decrease in risk with increasing dose for women exposed between ages 40 and 50. In absolute terms, the observed increase in excess cases per unit dose was approximately the same for survivors exposed during their second, third, and fourth decades of life but, for similar ages at observation for risk, those exposed at younger ages exhibited higher levels of excess risk. For women who developed breast cancer, mean time from exposure until cancer diagnosis was shown to be heavily dependent upon exposure age but independent of radiation dose. In the third LSS survey, through 1980, Tokunaga et al.7) ascertained 564 breast cancer cases in the LSS sample. The most remarkable findings) was a statistically significant dose response for 24 cases diagnosed among women who were under 10 years of age ATB. The relationship was seen even among women under 5 ATB, and provided the first strong evidence that breast cancer can be induced by irradiation of stem cells, well before breast budding. The overall pattern of a decreasing relative risk with increasing age at exposure was thus strengthened, as the earlier pattern was maintained among women over 10 years of age ATB and the dose-related relative risk in the 0-9 ATB group was, if anything, even higher than that in the 10-19 ATB cohort. However, the dose-related deficit observed earlier in the 40-49 ATB group was no longer apparent. Within restricted age-ATB intervals, excess relative risk tended to remain fairly constant over time following exposure; this is another manifestation of the observation, reported in the two earlier LSS surveys, that time from exposure until cancer diagnosis tends to be independent of radiation dose. Regardless of the age at exposure, no excess risk was apparent until ages at which rates in the non-exposed population become appreciable. At the time of the third survey, the dosimetric basis for estimation of risk in the LSS sample was being reevaluated, a process which eventually led to the DS86 dosimetry9,10) now in place. Based on preliminary information, it was calculated that the new dosimetry would result in an . increase of about 30% in dose-specific estimates of increased risk7) Breast cancer incidence in other irradiated populations Following Mackenzie's study, which was extended by Myrden and Hiltz11), Boice and Monson12) reported a dose-related excess risk among 1054 patients treated by pneumothorax and monitored with multiple fluoroscopies at a Massachusetts tuberculosis sanitorium; many of them had been treated as teenagers and a decreasing relative risk was observed with increasing exposure age similar to that seen in the LSS sample. More recently, Hrubec et al.13) have reported on follow-up through 1980; 58 cancers were observed vs. 35.8 expected based on general population rates, whereas 19 were observed vs. 22.8 expected among women treated by other means. Only 2 cancers were observed among women treated by pneumothorax before age 15, but the relative risk decreased from 3.0 (19 observed vs. 6.3 expected) for treatment beginning at ages 15-19, to 1.5 (25 vs 16.9) at ages 20-29, to barely one (9 vs. 8.2) for treatment beginning at ages 30-39. Dose-related excess breast cancer risk has also been observed among women treated by X ray for benign breast disease. Shore et al.14), in the most recent of a series of follow-up studies of a fixed cohort of New York women treated for acute postpartum mastitis14,15),found 56 breast cancers among 601 exposed patients compared to 59 among 1239 non-exposed controls. Eighty-five percent of the women were 20-34 years of age at the time of treatment; 4.5010 were younger and 10.3% were older. There was no significant difference by exposure age with respect to dose specific excess relative risk, which was 0.58±0.18 per Gy for breast doses under 7 Gy. No significant differences were found between irradiated and control subjects with respect to time from exposure or study enrollment to breast cancer diagnosis, and relative risk remained roughly constant over time following exposure. In 1983 Hildreth et al.16) reported a 5-fold increased risk of breast cancer among 1201 women who had received X-ray treatment in infancy for an enlarged thymus, as compared to their 2469 non-irradiated sisters. This finding confirmed and strengthened the inference by Tokunaga et a1.8) of a dose-related excess risk among female A-bomb survivors under age 10 ATB, the more so since more than 90% of the thymus patients had been less than 6 months of age at the time of their exposures. After another 6 more years of follow-up17 , the number of breast cancers increased from 9 to 22 in the irradiated group, and from 4 to 12 in their non irradiated sisters. The estimated excess relative risk at 1 Gy breast tissue dose was 2.48 (95% confidence interval 1.1 to 5.2). The first breast cancer was observed 28 years after exposure, and there was no difference between the irradiated and non-irradiated groups with respect to mean age at breast cancer diagnosis. A COMPARISON OF PUBLISHED FINDINGS A formal analysis in parallel18), using identical age groupings, follow-up intervals, and Table 1. Estimates of excess relative and absolute risk per Gy breast tissue dose , from Land et al.
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